The mechanism and consequence of ATP hydrolysis accompanying the polymerization of actin has been studied. We have found that ADP.actin polymerizes spontaneously similarly to ATP.actin. By greatly increasing the rate of polymerization of ATP.actin by sonication, we have proved that hydrolysis of ATP occurs as a subsequent step on the F-actin. The critical concentration and association and dissociation rate constants have been determined for actin polymerized in ATP and in ADP. The critical concentration in ADP is greater than in ATP because the association rate constant is lower and the dissociation rate constant is larger. The kinetic constants in ADP are, as expected for an equilibrium polymer, the same above and below the critical concentration. But in ATP, the filaments at steady state have and ATP-cap that stabilizes the polymer. As a result, when the ATP cap is lost dissociation occurs at the higher rate determined by the dissociation rate constant for ADP.actin. When the rate of formation of ADP.actin monomers exceeds the rate of exchange of ATP for ADP on the actin, ADP.actin accumulates and the rate of association is determined by the lower rate constant for ADP.actin. Thus, below its critical concentration or when filament number concentration is greatly increased the rate constants for ATP.actin approach those for ADP.actin. This phenomenon also applies at steady state where a statistical fraction of filaments will lose their ATP caps and rapidly depolymerize while ATP-capped filaments elongate in equivalent amount. Thus, the energy of hydrolysis of ATP stabilizes the actin filament, which contains mostly ADP.actin subunits and an ATP.actin cap, and allows regulation of the polymerization state through changes in the rates of individual steps in the polymerization process. Non-covalent modification of actin by virtue of associated ATP or ADP is, therefore, exactly analogous to covalent modification of proteins through phosphorylation and dephosphorylation.